Rin Okumura begins to worry about his future as his twin brother, Yukio, is starting school at the prestigious True Cross Academy. Sent to a job interview by his foster father, Shiro, Rin encounters a demon-like creature and causes havoc in the store.

Rin is thrown into turmoil when Shiro tells him that he's the son of Satan! Warning him that he must never draw it, Shiro gives Rin the Koma Sword, and hides him in the monastery basement. Outside, a fierce battle begins...

Vowing to become an exorcist, Rin is taken to True Cross Academy by the mysterious Mephisto, a friend of their late father. Later, Rin heads to the Exorcist Cram School, as Mephisto warns - 'You must keep that you're the son of Satan confidential.'

When Yukio takes on a case, Rin tags along with him to the Exorcism Supply Shop. There he meets Shiemi, a girl with ailing legs, tending to her garden. Yukio examines Shiemi's legs and finding demonic traces, speculates that the garden is the cause.

Rin is always snoozing in class, much to star pupil Suguro's irritation. Suguro's striving to become an exorcist so he can restore his family's temple in Kyoto, and being classmates with such a slacker is more than he can bear.

The biggest headache of Rin's school life is his daily meals. On Yukio's advice, Rin starts cooking in the dorm kitchen, preparing lunch the night before. But in the morning, all the food has vanished!

To overcome her shyness, Shiemi secretly vows to 'Make friends!' But she's foiled by her klutziness. After displaying her Tamer skills in class, she finally asks Izumo to be her friend! Soon after, the Exorcist Cram School holds a boot camp.

Crushed by her failure to save her best friend, Izumo lashes out at Suguro! Their bickering escalates until the whole class is involved, and they're all sent to detention. Suddenly, the students are attacked by the ghoul Rin fought the day before!

Fighting together for the first time, Rin and the others barely survive a harrowing attack. Suddenly, Mephisto and the cram school teachers are before them! Sensing something odd in Noihaus's behavior, Yukio confronts the teacher, only to discover...

After the excitement of being promoted to ExWire, Rin is soon disgusted with his load of homework. Then, Yukio is summoned for an urgent mission! The familiar of the Knights of the True Cross has gone berserk, and Yukio has to deal with the crisis.

Rin, Shima and Izumo have been sent on a mission, only to end up working instead. They meet a boy named Yohei and learn of the "Demon of the Deep." Yohei lost his father to this monster, and wants revenge. Worried, Rin and the others watch over him.

The class investigates ghost sightings at an amusement park. Rin is partnered with Shiemi, and they find the ghost of a child. He runs away, turning things into a game of tag! Separated from Shiemi, Rin is confronted by Amaimon, King of Earth.

Senior Exorcist First Class Shura Kirigakure stops the battle between Rin and Amaimon. Rin learns that Shura was once a disciple of Shiro's - and that Shura has targeted him for elimination - "the job that my mentor failed to do!"

The first semester has ended, signaling the start of summer vacation for True Cross Academy students. But there's no rest in sight for Rin and the other ExWires: first they must take part in a 3-day drill to prepare them for actual combat, under the guise of a camping trip out in the forest.

Consumed by the power of the flames during his battle with Amaimon, Rin goes berserk. He regains control of himself once his power is exhausted, only to be captured then and there by the current Paladin, Angel.

Rin is undergoing training so that he can learn to master his demonic flames. Just then, a giant bird-like demon called Gufu swoops in on him! With Yukio's help, he drives it away, but all of the Cram School members are sent to investigate how the demon infiltrated the academy... Suguro and the others are still investigating when Konekomaru appears, begging for help, with Rin in pursuit. According to Rin, Konekomaru's been possessed by a demon, but no one else can see it. Suguro, mistakenly believing that Rin is attacking Konekomaru, turns on him with hostility!

The Exorcism Cram School students are having a ball with Shima's birthday-based fortune-telling. When they discover that Izumo's birthday is coming up, they hit upon the idea of throwing her a surprise party.

Southern Cross Monastery, where Rin and Yukio grew up, has come under attack by a mysterious assailant. Leaving behind these cryptic words: "I will never forgive anyone related to Satan," the masked assailant escapes.

The assailant has escaped, but the monastery attack case is winding down. Just then, an elderly man calling himself Ernst appears before Yukio. He reveals the secret of Yukio and Rin's birth, as well as what the Vatican did their mother. Shocked, Yukio also begins to harbor doubts about the Knights of the True Cross. Meanwhile, the injured assailant has stumbled into Shiemi's garden at the Supply Shop...

In light of the incidents following the monastery attack, Mephisto is dismissed from his post as director. The Order's Supreme Advisors, the Grigori, are ousted as well, paving the way for Ernst to become Pope. And the newly appointed Preceptor of the Japan Branch is revealed to be...

Hordes of demons are spilling out of Gehenna Gate! And these intruders from the "Empty World" are now indiscriminately attacking the people of True Cross Academy Town! Meanwhile, on the roof of the school building, Rin has been rescued by Suguro and Shiemi and is starting to come to. What Rin sees when he awakens is...

Satan has transformed himself into a gigantic Gehenna Gate, and is attempting to absorb all of Assiah by expanding a rip in the dimension. Rin and Yukio, joined by Shura and Angel, attack the gate, but it's an uphill battle against Satan's overwhelming power. Meanwhile, at the school, the exorcists are in a desperate situation, as a myriad of demons attack. Just then, Suguro proposes a strategy for a comeback! But will it work? Rousing themselves into action one last time, Rin and Yukio head toward the gate. To protect their beloved friends, and this world!